The insulin-like growth factor I (IGF-I) within the bony fish pituitary: New morphofunctional and phylogenetic aspects

Open Neuroendocrinology Journal

Volumn 4, Issue SPEC. ISSUE 1, 2011, Pages 43-50

  Eppler, Elisabeth ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

MSH; ACTH; Adenohypophysis; Feed back mechanism; FSH; GH; Gonadotroph; IGF I; Intrapituitary loop; LH; Neurohypophysis; Ontogeny; Phylogeny; Prolactin; Somatotroph; TSH

Indexed keywords

SOMATOMEDIN C;

ACTH SECRETING CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELL FUNCTION; CELL PROLIFERATION; CELL STIMULATION; CELL VIABILITY; FEEDBACK SYSTEM; GENETIC CONSERVATION; GONADOTROPIN SECRETING CELL; GROWTH HORMONE SECRETING CELL; HYPOPHYSIS FUNCTION; MOLECULAR DYNAMICS; MOLECULAR PHYLOGENY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN STRUCTURE; SEX DIFFERENCE; SPECIES COMPARISON; STRUCTURE ACTIVITY RELATION; TILAPIA; TSH SECRETING CELL;

EID: 80455156285     PISSN: None     EISSN: 18765289     Source Type: Journal    
DOI: 10.2174/1876528901104010043     Document Type: Article

References (99)

1. Jones JI, Clemmons DR. Insulin-like growth factors and their binding proteins: biological actions. Endocr Rev 1995; 16: 3-34.
2. Reinecke M, Schmid AC, Heyberger-Meyer B, Hunziker EB, Zapf J. Effect of growth hormone and insulin-like growth factor I (IGFI) on the expression of IGF-I messenger ribonucleic acid and peptide in rat tibial growth plate and articular chondrocytes in vivo. Endocrinology 2000; 141: 2847-2853.
3. Fletcher TP, Thomas GB, Dunshea FR, Moore LG, Clarke IJ. IGF feedback effects on growth hormone secretion in ewes: evidence for action at the pituitary but not the hypothalamic level. J Endocrinol 1995; 144: 323-331.
4. Niiori-Onishi A, Iwasaki Y, Mutsuga N, Oiso Y, Inoue K, Saito H. Molecular mechanisms of the negative effect of insulin-like growth factor-I on growth hormone gene expression in MtT/S somatotroph cells. Endocrinology 1999; 140: 344-349.
5. Wallenius K, Sjogren K, Peng XD, et al. Liver-derived IGF-I regulates GH secretion at the pituitary level in mice. Endocrinology 2001; 142: 4762-4770.
6. David I, Bosshard R, Kloas W, Reinecke M. Insulin-like growth factor I (IGF-I) in the pituitary of Xenopus laevis: Immunocytochemical and autoradiographic indication for a paracrine action and co-release with prolactin. J Neuroendocrinol 2000; 12: 415-420.
7. Rosenfeld RG, Ceda G, Wilson DM, Dollar LA, Hoffman AR. Characterization of high affinity receptors for insulin-like growth factors I and II on rat anterior pituitary cells. Endocrinology 1984; 114: 1571-1575.
8. Werther GA, Hogg A, Oldfield BJ, et al. Localization and characterization of insulin receptors in rat brain and pituitary gland using in vitro autoradiography and computerized densitometry. Endocrinology 1987; 121: 1562-1570.
9. Olchovsky D, Song J, Gelato MC, et al. Pituitary and hypothalamic insulin-like growth factor-I (IGF-I) and IGF-I receptor expression in food-deprived rats. Mol Cell Endocrinol 1993; 93: 193-198.
10. Eppler E, Jevdjovic T, Maake C, Reinecke M. Morphology and molecular biology of insulin-like growth factor I (IGF-I) and its receptor IGF-1R in the rat anterior pituitary. Eur J Neurosci 2007a; 25: 191-200.
11. Adam CL, Gadd TS, Findlay PA, Wathes DC. IGF-I stimulation of luteinizing hormone secretion, IGF-binding proteins (IGFBPs) and expression of mRNAs for IGFs, IGF receptors and IGFBPs in the ovine pituitary gland. J Endocrinol 2000; 166: 247-254.
12. Oomizu S, Takeuchi S, Takahashi S. Stimulatory effect of insulinlike growth factor I on proliferation of mouse pituitary cells in serum-free culture. J Endocrinol 1998; 157: 53-62.
13. Yamamoto H, Prager D, Yamasaki H, Melmed S. Rat pituitary GC cell insulin-like growth factor-I receptor regulation. Endocrinology 1993; 133: 1420-1425.
14. Honda J, Takeuchi S, Fukamachi H, Takahashi S. Insulin-like growth factor-I and its receptor in mouse pituitary glands. Zool Sci 1998; 4: 573-579.
15. Reinecke M, Collet C. The phylogeny of the insulin-like growth factors. Int Rev Cytol 1998; 183: 1-94.
16. Reinecke M, Björnsson BT, Dickhoff WW, et al. Growth hormone and insulin-like growth factors in fish: where we are and where to go. Gen Comp Endocrinol 2005; 142: 20-24.
17. Reinecke M. Insulin and the insulin-like growth factors. In: Reinecke M, Zaccone G, Kapoor BG, eds. Fish Endocrinology. Enfield (NH), Jersey, Plymouth, USA: Science Publishers, 2006, Vol. 1: 3-13.
18. Bach MA, Bondy CA. Anatomy of the pituitary insulin-like growth factor system. Endocrinology 1992; 131: 2588-2594.
19. Olchovsky D, Bruno JF, Gelato MC, Song J, Berelowitz M. Pituitary insulin-like growth factor-I content and gene expression in the streptozotocin-diabetic rat: evidence for tissue-specific regulation. Endocrinology 1991; 128: 923-928.
20. González-Parra S, Argente J, Chowen JA, et al. Gene expression of the insulin-like growth factor system during postnatal development of the rat pituitary gland. J Neuroendocrinol 2001; 13: 86-93.
21. Alberti VN, Takita LC, de Mesquita IS, Percario S, Maciel RMB. Immunohistochemical demon-stration of insulin-like growth factor I (IGF-I) in normal and pathological human pituitary glands. Pathol Res Pract 1991; 187: S41-S42.
22. Jevdjovic T, Bernays R, Eppler E. Insulin-like growth factor I (IGF-I) mRNA and peptide in the human anterior pituitary. J Neuroendocrinol 2007; 19: 335-341.
23. Michels KM, Lee WH, Seltzer A, Saavedra JM, Bondy CA. Upregulation of pituitary [125I]insulin-like growth factor-I (IGF-I) binding and IGF binding protein-2 and IGF-I gene expression by estrogen. Endocrinology 1993; 132: 23-29.
24. Ren P, Schelthauer BW, Halper J. Immunohistological localization of TGFalpha, RGF, IGF-I, and TGFbeta in the normal human pituitary gland. Endocr Pathol 1994; 5: 40-48.
25. Eppler E, Shved N, Moret O, Reinecke M. IGF-I is distinctly located in the bony fish pituitary as revealed for Oreochromis niloticus, the Nile tilapia, using real-time RT-PCR, in situ hybridisation and immunohistochemistry. Gen Comp Endocrinol 2007b; 150: 87-95.
26. Melmed S, Yamashita S, Yamasaki H, et al. IGF-I receptor signalling: lessons from the somatotroph. Rec Progr Horm Res 1996; 51: 189-215.
27. Honda J, Manabe Y, Matsumura R, Takeuchi S, Takahashi S. IGFI regulates pro-opiomelanocortin and GH gene expression in the mouse pituitary gland. J Endocrinol 2003; 178: 71-82.
28. Wong AOL, Zhou H, Jiang Y, Ko, WKW. Feedback regulation of growth hormone synthesis and secretion in fish and the emerging concept of intrapituitary feedback loop. Comp Biochem Physiol A 2006; 144: 284-305.
29. Renner U, Mojto J, Arzt E, Lange M, Stalla J, Muller OA, Stalla GK. Secretion of polypeptide growth factors by human nonfunctioning pituitary adenoma cells in culture. Neuroendocrinology 1993; 57: 825-834.
30. Wingstrand KG. Comparative anatomy and evolution of the hypophysis. In: Harris GW, Donovan BT, Eds. The pituitary gland, London, UK: Butterworths, 1966, Vol. 1: 58-126.
31. Holmes RL, Ball JN. The pituitary gland - a comparative account. London, New York, USA: Cambridge University Press; 1974.
32. Weltzien FA, Andersson E, Andersen Ø, Shalchian-Tabrizi K, Norberg B. The brain-pituitary-gonad axis in male teleosts, with special emphasis on flatfish (Pleuronectiformes). Comp Biochem Physiol A 2004; 137: 447-477.
33. Agulleiro B, García-Hernández MP, García Ayala A. Teleost adenohypophysis: morphofunctional and developmental aspects. In: Reinecke M, Zaccone G, Kapoor BG, eds. Fish Endocrinology. Enfield (NH), Jersey, Plymouth, USA: Science Publishers, 2006, Vol. 1: pp. 289-323.
34. Kasper RS, Shved N, Takahashi A, Reinecke M, Eppler E. A systematic immunohistochemical survey on the distribution patterns of growth hormone, prolactin, somatolactin, ß-TSH, ß- FSH, ß-LH, ACTH, and α-MSH in the adenohypophysis of Oreochromis niloticus, the Nile tilapia. Cell Tissue Res 2006; 325: 303-313.
35. Inoue K, Iwatani H, Takei Y. Growth hormone and insulin-like growth factor I of a Euryhaline fish Cottus kazika: cDNA cloning and expression after seawater acclimation. Gen Comp Endocrinol 2003; 131: 77-84.
36. Lynn SG, Shepherd BS. Molecular characterization and sexspecific tissue expression of prolactin, somatolactin and insulin-like growth factor-I in yellow perch (Perca flavescens). Comp Biochem Physiol B Biochem Mol Biol 2007; 147: 412-427.
37. Filby AL, Tyler CR. Cloning and characterization of cDNAs for hormones and/or receptors of growth hormone, insulin-like growth factor-I, thyroid hormone, and corticosteroid and the gender-, tissue-, and developmental-specific expression of their mRNA transcripts in fathead minnow (Pimephales promelas). Gen Comp Endocrinol 2007; 150: 15-63.
38. Wang DS, Jiao B, Hu C, Huang X, Liu Z, Cheng CH. Discovery of a gonad-specific IGF subtype in teleost. Biochem Biophys Res Comm 2008; 367:336-341.
39. Davis LK, Pierce AL, Hiramatsu N, Sullivan CV, Hirano T, Grau EG. Gender-specific expression of multiple estrogen receptors, growth hormone receptors, insulin-like growth factors and vitellogenins, and effects of 17 beta-estradiol in the male tilapia (Oreochromis mossambicus). Gen Comp Endocrinol 2008; 156:544-551.
40. Eppler E, Berishvili G, Mazel P, et al. Distinct organ-specific upand downregulation of IGF-I and IGF-II mRNA in various organs of a GH-overexpressing transgenic Nile tilapia. Transgenic Res 2010; 19:231-240.
41. Melamed P, Gur G, Rosenfeld H, Elizur A, Yaron Z. Possible interactions between gonadotrophs and somatotrophs in the pituitary of the tilapia: apparent roles for insulin-like growth factor I and estradiol. Endocrinology 1999; 140: 1183-1191.
42. Moret O, Berishvili G, Shved N, et al. Insulin-like growth factor I (IGF-I) mRNA and peptide in the hypothalamic-pituitary-gonadal axis during development of the tilapia, Oreochromis niloticus. CYBIUM, Int J Ichthyol 2008; 32(2 Suppl.): 31-33.
43. Shved N, Baroiller J-F, Eppler E. Further insights into the insulinlike growth factor-I system of bony fish pituitary with special emphasis on reproductive phases and social status. Ann NY Acad Sci 2009; 1163: 517-520.
44. Somoza GM, Miranda LA, Strobl-Mazzulla P, Guilgur LG. Gonadotropin-releasing hormone (GnRH): from fish to mammalian brains. Cell Mol Neurobiol 2002; 22:589-609.
45. Parhar IS, Soga T, Ogawa S, Sakuma Y. FSH and LH-ß subunits in the preoptic nucleus: ontogenic expression in teleost. Gen Comp Endocrinol 2003; 132: 369-378.
46. Berishvili G, Shved N, Eppler E, Clota F, Baroiller J-F, Reinecke M. Organ-specific expression of IGF-I during early development of bony fish as revealed in the tilapia, Oreochromis niloticus, by in situ hybridization and immunohistochemistry: indication for the particular importance of local IGF-I. Cell Tissue Res 2006a; 325: 287-301.
47. Takahashi A, Kobayashi Y, Amano M, Yamanome T. Structural and functional diversity of proopiomelanocortin in fish with special reference to barfin flounder. Peptides 2009; 30: 1374-1382.
48. Schmidt WK, Moore HP. Synthesis and targeting of insulin-like growth factor-I to the hormone storage granules in an endocrine cell line. J Biol Chem 1994; 269: 27115-27124.
49. Schmid AC, Lutz I, Kloas W, Reinecke M. Thyroid hormone stimulates hepatic IGF-I mRNA expression in a bony fish, the tilapia Oreochromis mossambicus, in vitro and in vivo. Gen Comp Endocrinol 2003; 130:129-134.
50. Saga T, Oota Y, Nozaki M, Swanson P. Salmonid pituitary gonadotrophs. III. Chronological appearance of GTH I and other adenohypophysial hormones in the pituitary of the developing rainbow trout (Oncorhynchus mykiss irideus). Gen Comp Endocrinol 1993; 92: 233-241.
51. Laiz-Carrión R, del Mar Segura-Noguera M, Martín del Río MP, Mancera JM. Ontogeny of adenohypophyseal cells in the pituitary of the American shad (Alosa sapidissima). Gen Comp Endocrinol 2003; 132: 454-464.
52. Berishvili G, D'Cotta H, Baroiller J-F, Segner H, Reinecke M. Differential expression of IGF-I mRNA and peptide in the male and female gonad during early development of a bony fish, the tilapia Oreochromis niloticus. Gen Comp Endocrinol 2006b; 146: 204-210.
53. Degani G, Goldberg D, Tzchori I, Hurvitz A, Yom Din S, Jackson K. Cloning of European eel (Anguilla anguilla) FSH-β subunit, and expression of FSH-β and LH-β in males and females after sex determination. Comp Biochem Physiol B 2003; 136: 283-293.
54. Burmeister SS, Kailasanath V, Fernald RD. Social dominance regulates androgen and estrogen receptor gene expression. Horm Behav 2007; 51: 164-170.
55. Pazos F, Sanchez-Franco F, Balsa J, Escalada J, Cacicedo L. Differential regulation of gonadotropins and glycoprotein hormone alpha-subunit by IGF-I in anterior pituitary cells from male rats. J Endocrinol Invest 2004; 27: 670-675.
56. Kanematsu T, Irahara M, Miyake T, Shitsukawa K, Aono T. Effect of insulin-like growth factor I on gonadotropin release from the hypothalamus-pituitary axis in vitro. Acta Endocrinol (Copenh) 1991; 125: 227-233.
57. Soldani R, Cagnacci A, Yen SS. Insulin, insulin-like growth factor I (IGF-I) and IGF-II enhance basal and gonadotrophin-releasing hormone-stimulated luteinizing hormone release from rat anterior pituitary cells in vitro. Eur J Endocrinol 1994; 131: 641-645.
58. Soldani R, Cagnacci A, Paoletti AM, Yen SS, Melis GB. Modulation of anterior pituitary luteinizing hormone response to gonadotropin-releasing hormone by insulin-like growth factor I in vitro. Fertil Steril 1995; 64: 634-637.
59. Xia YX, Weiss JM, Polack S, Diedrich K, Ortmann O. Interactions of insulin-like growth factor-I, insulin and estradiol with GnRH stimulated luteinizing hormone release from female rat gonadotrophs. Eur J Endocrinol 2001; 144: 73-79.
60. Whitley NC, Barb CR, Utley RV, Popwell JM, Kraeling RR, Rampacek GB. Influence of stage of the estrous cycle on insulinlike growth factor-I modulation of luteinizing hormone secretion in the gilt. Biol Reprod 1995; 53: 1359-1364.
61. Chang JP, Johnson JD, Sawisky GR, et al. Signal transduction in multifactorial neuroendocrine control of gonadotropin secretion and synthesis in teleosts-studies on the goldfish model Gen Comp Endocrinol 2009; 161: 42-52.
62. Reinecke M. Insulin-like growth factors and fish reproduction. Biol Reprod 2010; 82: 656-661.
63. Huang YS, Rousseau K, Le Belle N, et al. Insulin-like growth factor-I stimulates gonadotrophin production from eel pituitary cells: a possible metabolic signal for induction of puberty. J Endocrinol 1998; 159: 43-52.
64. Baker DM, Davies B, Dickhoff WW, Swanson P. Insulin-like growth factor I increases follicle-stimulating hormone (FSH) content and gonadotropin-releasing hormone-stimulated FSH release from coho salmon pituitary cells in vitro. Biol Reprod 2000; 63: 865-871.
65. Rosenfeld H, Levavi-Sivan B, Gur G, et al. Characterization of tilapia FSHbeta gene and analysis of its 5' flanking region. Comp Biochem Physiol B 2001; 129: 389-398.
66. Lin S-W, Ge W. Differential regulation of gonadotropins (FSH and LH) and growth hormone (GH) by neuroendocrine, endocrine, and paracrine factors in the zebrafish - An in vitro approach. Gen Comp Endocrinol 2009; 160: 183-193.
67. Ando H, Luo Q, Koide N, Okada N, Urano A. Effects of insulinlike growth factor I on GnRH-induced gonadotropin subunit gene expressions in masu salmon pituitary cells at different stages of sexual maturation. Gen Comp Endocrinol 2006; 149: 21-29.
68. Furukuma S, Onuma T, Swanson P, et al. Stimulatory effects of insulin-like growth factor 1 on expression of gonadotropin subunit genes and release of follicle-stimulating hormone and luteinizing hormone in masu salmon pituitary cells early in gametogenesis. Zool Sci 2008; 25: 88-98.
69. Weil C, Carré F, Blaise O, Breton B, le Bail P-Y. Differential effects of insulin-like growth factor I on in vitro gonadotropin (I and II) and growth hormone secretions in rainbow trout (Oncorhynchus mykiss) at different stages of the reproductive cycle. Endocrinology 1999; 140: 2054-2062.
70. le Roith D, Roberts CT Jr. The insulin-like growth factor system and cancer. Cancer Lett 2003; 195: 127-137.
71. Fernández M, Sánchez-Franco F, Palacios N, Sánchez I, Fernández C, Cacicedo L. IGF-I inhibits apoptosis through the activation of the phospatidylinositol 3-kinase/Akt pathway in pituitary cells. J Mol Endocrinol 2004; 33: 155-163.
72. Gianotti L, Ramunni J, Lanfranco F, et al. Recombinant human IGF-I does not modify the ACTH and cortisol responses to hCRH and hexarelin, a peptidyl GH secretagogue, in humans. J Endocrinol Invest 2001; 24: 67-71.
73. Goodyer CG, de Stephano L, Guyda HJ, Posner BI. Effects of insulin-like growth factors on adult male rat pituitary function in tissue culture. Endocrinology 1984; 115: 1568-1576.
74. Lu F, Yang K, Han VK, Challis JR. Expression, distribution, regulation and function of IGFs in the ovine fetal pituitary. J Mol Endocrinol 1995; 14: 323-336.
75. Verburg-Van Kemenade BML, Stolte EH, Metz JR, Chadzinska M. Neuroendocrine-immune interactions in teleost fish. In: Bernier NJ, Van der Kraah G, Farrell AP, Brauner CJ, Eds: Fish Physiol 2009; 28: 313-364.
76. Abe H, Molitch ME, van Wyk JJ, Underwood LE. Human growth hormone and somatomedin C suppress the spontaneous release of growth hormone in unanesthetized rats. Endocrinology 1983; 113: 1319-1324.
77. Tannenbaum GS, Guyda HJ, Posner BI. Insulin-like growth factors: a role in growth hormone negative feedback and body weight regulation via brain. Science 1983; 220: 77-79.
78. Sheppard MS, Bala RM. Insulin-like growth factor inhibition of growth hormone secretion. Can J Physiol Pharmacol 1986; 64: 525-530.
79. Yamashita S, Melmed S. Effects of insulin on rat anterior pituitary cells. Inhibition of growth hormone secretion and mRNA levels. Diabetes 1986; 35: 440-447.
80. Simes JM, Wallace JC, Walton PE. The effects of insulin-like growth factor-I (IGF-I), IGF-II and des(1-3)IGF-I, a potent IGF analogue, on growth hormone and IGF-binding protein secretion from cultured rat anterior pituitary cells. J Endocrinol 1991; 130: 93-99.
81. Lara JI, Lorenzo MJ, Cacicedo L, et al. Induction of vasoactive intestinal peptide gene expression and prolactin secretion by insulin- like growth factor I in rat pituitary cells: evidence for an autoparacrine regulatory system. Endocrinology 1994; 135: 2526-2532.
82. Atkin SL, Landolt AM, Foy P, Jeffreys RV, Hipkin L, White MC. Effects of insulin-like growth factor-I on growth hormone and prolactin secretion and cell proliferation of human somatotrophinomas and prolactinomas in vitro. Clin Endocrinol 1994; 41: 503-509.
83. Castillo AI, Aranda A. Differential regulation of pituitary-specific gene expression by insulin-like growth factor 1 in rat pituitary GH4C1 and GH3 cells. Endocrinology 1997; 138: 5442-5451.
84. Fruchtman S, Jackson L, Borski R. Insulin-like growth factor I disparately regulates prolactin and growth hormone synthesis and secretion: studies using the teleost pituitary model. Endocrinology 2000; 141: 2886-2894.
85. Cameron C, Moccia RD, Leatherland JF. Growth hormone secretion from the Arctic charr (Salvelinus aplinus) pituitary gland in vitro: effects of somatostatin-14, insulin-like growth factor-I, and nutritional status. Gen Comp Endocrinol 2005; 141: 93-100.
86. Perez-Sanchez J, Weil C, Le Bail PY. Effects of human insulin-like growth factor-I on release of growth hormone by rainbow trout (Oncorhynchus mykiss) pituitary cells. J Exp Zool 1992; 262: 287-290.
87. Rousseau K, Huang YS, Le Belle N, et al. Long-term inhibitory effects of somatostatin and insulin-like growth factor 1 on growth hormone release by serum-free primary culture of pituitary cells from European eel (Anguilla anguilla). Neuroendocrinology 1998; 67: 301-319.
88. Picha ME, Strom CN, Riley LG, Walker AA, Won ET, Johnstone WM, Borski RJ. Plasma ghrelin and growth hormone regulation in response to metabolic state in hybrid striped bass: effects of feeding, ghrelin and insulin-like growth factor-I on in vivo and in vitro GH secretion. Gen Comp Endocrinol 2009; 161:365-372.
89. Raven PA, Uh M, Sakhrani D, et al. Endocrine effects of growth hormone overexpression in transgenic coho salmon. Gen Comp Endocrinol 2008; 159:26-37.
90. Eppler E, Caelers A, Shved N, et al. Insulin-like growth factor I (IGF-I) in a growth-enhanced transgenic (GH-overexpressing) bony fish, the tilapia (Oreochromis niloticus): indication for a higher impact of autocrine/paracrine than of endocrine IGF-I. Transgenic Res 2007c;16:479-489.
91. Caelers A, Maclean N, Hwang G, Eppler E, Reinecke M. Expression of endogenous and exogenous growth hormone (GH) in a GH-transgenic tilapia (Oreochromis niloticus). Transgenic Res 2005; 14: 95-104.
92. Pierce AL, Dickey JT, Larsen DA, Fukada H, Swanson P, Dickhoff WW. A quantitative real-time RT-PCR assay for salmon IGF-I mRNA, and its application in the study of GH regulation of IGF-I gene expression in primary culture of salmon hepatocytes. Gen Comp Endocrinol 2004; 135:401-411.
93. Uchida K, Kajimura S, Riley LG, Hirano T, Aida K, Grau EG. Effects of fasting on growth hormone/insulin-like growth factor I axis in the tilapia, Oreochromis mossambicus. Comp Biochem Physiol A Mol Integr Physiol 2003; 134:429-439.
94. Sjögren K, Liu JL, Blad K, et al. Liver-derived insulin-like growth factor I (IGF-I) is the principal source of IGF-I in blood but is not required for postnatal body growth in mice. Proc Natl Acad Sci USA 1999; 96:7088-7092.
95. Yakar S, Liu JL, Stannard B, et al. Normal growth and development in the absence of hepatic insulin-like growth factor I. Proc Natl Acad Sci U S A 1999; 96:7324-7329.
96. Shved N, Berishvili G, Baroiller J-F, Segner H, Eppler E, Reinecke M. Ethinylestradiol differentially interferes with the IGF-I system in the tilapia, Oreochromis niloticus. J Endocrinol 2007; 195: 513-523.
97. Shved N, Berishvili G, Baroiller JF, Segner H, Reinecke M. Environmentally relevant concentrations of 17alphaethinylestradiol (EE2) interfere with the growth hormone (GH)/insulin-like growth factor (IGF)-I system in developing bony fish. Toxicol Sci 2008; 106: 93-102.
98. Chowen JA, Frago LM, Argente J. The regulation of GH secretion by sex steroids. Review. Eur J Endocrinol 2004; 151 (Suppl 3): U95-U100.
99. Jorgensen JO, Christensen JJ, Krag M, Fisker S, Ovesen P, Christiansen JS. Serum insulin-like growth factor I levels in growth hormone-deficient adults: influence of sex steroids. Horm Res 2004; 62 (Suppl 1): 73-76.